Graziella Borges AlvesI; Elisa Teruya OshiroII; Marcio da Cruz LeiteIII; Aline Vidor MelãoIII; Letícia Moraes RibeiroII; Nathália Lopes Fontoura MateusII; Reginaldo Peçanha BrazilIV; José Dilermando Andrade FilhoV; Alessandra Gutierrez de OliveiraI,II
IPrograma de Pós-Graduação em Doenças Infecciosas e Parasitárias, Universidade Federal do Mato Grosso do Sul, Campo Grande, MS IILaboratório de Parasitologia Humana, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Mato Grosso do Sul, Campo Grande, MS IIICurso de Ciências Biológicas, Universidade Estadual de Mato Grosso, Cáceres, MT IVDepartamento de Bioquímica e Biologia Molecular, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, RJ VColeção de Flebotomíneos, Centro de Referência Nacional e Internacional para Flebotomíneos, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte, MG
ABSTRACT
INTRODUCTION: Leishmaniasis is expanding across Brazil, including the State of Mato Grosso (MT). The aim of this study was to characterize the phlebotomine sandfly fauna at threerural settlements located in the municipality of Cáceres, MT, from August 2010 to July 2011.
METHODS: Sandfly captures were conducted at the forest border and in intra and peridomicile areas with automatic light traps, biweekly, from 5pm to 6am.
RESULTS: Of the 630 sandflies collected, 348 were female, and 282 were male. Captured specimens were distributed across 11 genera – Brumptomyia, Evandromyia, Expapillata, Lutzomyia, Martinsmyia, Micropygomyia, Nyssomyia, Pintomyia, Psathyromyia, Psychodopygus, and Sciopemyia – and 28 species. Among these, six species had not been marked yet in MT (Brumptomyia avellari, Br. mangabeirai, Evandromyia aldafalcaoae, Micropygomyia echinatopharynx, Micropygomyia peresi, and Pa. campograndensis). Nyssomyia whitmani was the most abundant species across ecotopes at all settlements. Interestingly, Lutzomyia longipalpis and Lutzomyia cruzi were found in sympatry.
CONCLUSIONS: The disorganized occupation of the environment that is happening at the rural settlements of Mata Comprida, Laranjeira I and II could provide opportunities for the domiciliation of wild populations of phlebotomine, including vectors of leishmaniasis. Therefore, more studies are needed to understand the epidemiology of the disease in these areas and its impact on the human population.
Keywords: Mato Grosso. Phlebotomine fauna. Nyssomyia whitmani. Rural settlement.
RESUMO
INTRODUÇÃO: As leishmanioses encontram-se em expansão no Brasil, inclusive no Estado de Mato Grosso (MT). A presente pesquisa teve como objetivo estudar a fauna flebotomínica emtrês assentamentos rurais localizados no município de Cáceres, MT, entre agosto de 2010 e julhode 2011.
MÉTODOS: As coletas foram realizadas na margem da mata, no intra e peridomicílio com armadilhas automáticas luminosas, quinzenalmente, das 17h às 6h.
RESULTADOS: Foram coletados 630 exemplares, sendo 348 fêmeas e 282 machos. Os espécimes foramdistribuídos em 11 gêneros: Brumptomyia, Evandromyia, Expapillata, Lutzomyia, Martinsmyia,Micropygomyia, Nyssomyia, Pintomyia, Psathyromyia, Psychodopygus e Sciopemyia e 28 espécies, sendo que dentre estas, seis não haviam sido assinaladas em MT (Brumptomyia avellari, Br. mangabeirai, Evandromyia aldafalcaoae, Micropygomyia echinatopharynx, Micropygomyia peresi e Pa. campograndensis). Ressalta-se o encontro de Nyssomyia whitmani,espécie mais abundante nos diferentes ecótopos em todos os assentamentos. Destaca-se também a presençadas espécies Lutzomyia longipalpis e Lutzomyia cruzi em simpatria.
CONCLUSÕES: A ocupação desordenada do ambiente, como vem ocorrendo nos assentamentos Mata Comprida, LaranjeiraI e II, pode proporcionar a domiciliação de populações selváticas de flebotomíneos, dentre estes os vetores das leishmanioses, tornando-se necessários maiores estudos para entender a dinâmica de transmissão dessas morbidades nestes locais.
Palavras-chaves: Mato Grosso. Fauna flebotomínea. Nyssomyia whitmani. Assentamento rural.
INTRODUCTION
Leishmaniases are zoonoses transmitted by phlebotomine sandflies (Diptera: Psychodidae)1,2 and caused by parasites of the genus Leishmania, which can parasitize different orders of mammals. Human infection occurs as a consequence of the ecological relationship between parasites and vectors. Therefore, any change in the environment can result in modifications of the parasite distribution3.
In the State of Mato Grosso (MT), the presence of the following species has been reported: Lutzomyia cruzi, Lutzomyia longipalpis, and Lutzomyia whitmani. They were found in three biomes (Amazon rainforest, savannah, and Pantanal)4. All the 141 cities from the State have recorded autochthonous cases of the integumental form of the disease in these three ecosystems5, and the human visceral form is distributed in 34 municipalities of the State of Mato Grosso, with higher prevalence in the south-central and southeast regions of the State6.
Given the growing incidence and geographic spread of leishmaniasis, as well as the importance of the phlebotomine sandflies in the transmission of Leishmania species, this research aimed to analyze the phlebotomine sandfly fauna (Diptera: Psychodidae) in three rural settlements at the municipality of Cáceres, State of Mato Grosso, with a view to developing better control measures.
METHODS
Cáceres is 209.7km from the State capital, Cuiabá, and has the coordinates, S 16º 13′ 42″ W 57º 40′ 51″. The city has an altitude of 118m above sea level7. It is located in the south of the State and east of the Paraguai River and has an area of 24,351,446km2, an estimated urban population of 87,942 inhabitants, and three biomes: savannah, Amazon, and Pantanal8.
The mean annual temperature is 22.6ºC, and the climate is more pleasant in July with mean temperature of 19.1ºC. January is hot with a mean temperature of 26.4ºC. The city presents annual pluvial precipitation of 1,370mm, with the rainy season occurring between October and March, and in the other months, the climate becomes very dry. Humidity can reach up to 10% in August8.
This study was conducted from August 2010 to July 2011 at three rural settlements, Laranjeiras I and II, and Mata Comprida in the municipality of Cáceres (Figure 1). The settlements are located in the northwest of the State of Mato Grosso, near the BR 070 Cuiabá-Porto Velho highway, at the west side of Mangaval mountain range, 70km away from the urban area of the municipality. The occupied area of Laranjeira I, which was founded in 1988, is 108,523,712km2, and Pantanal biome is the prevalent vegetation. Laranjeira II holds an area of 11,928,120km2 and was founded in 19879. Mata Comprida has 34,448,425km2 and was founded in 1988 (PA Cunha: personal communication, 2011). The latter two places are characterized as savannah10.
In each settlement, three houses were chosen at random. Each had animals (dogs, chickens, pigs, horses, and others) and is near a forest. The captures were conducted at the forest border, and intra and peridomicile areas were with automatic light traps (Falcão model)11, biweekly, from 5pm to 6am.
Captured sandflies were sent to the laboratories of the Regional Health Office of Cáceres (ERSC) and Human Parasitology Laboratory of the Federal University of Mato Grosso do Sul (UFMS), separated, clarified, mounted, and identified according to the nomenclature of Galati2. The abbreviations of the genus follow the proposal of Marcondes12.
For the evaluation of the most abundant species as well as its spatial distribution, the index of species abundance was converted into a zero-to-one scale through the Standardized Index of Species Abundance (SISA). In this index, value 1 corresponds to the most abundant species13. The comparison of the frequencies among the phlebotomine populations, for the different regions and ecotopes, was conducted using chi-squared tests (χ2 for the contingency and absolute frequency tables).
RESULTS
Six hundred and forty-eight biweekly captures were conducted in the settlements of Laranjeira I, Laranjeira II, and Mata Comprida. Of the 630 specimens collected, 348 were females and 282 were males. Table 1 shows the distribution of the phlebotomine fauna present at these three settlements.
The total male: female ratio was 0.81:1, and the most abundant species collected in three settlements were 0.92:1 for Nyssomyia whitmani, 0.94:1 for Evandromyia evandroi, and 0.19:1 for Evandromyia termitophila.
Of the 29 species analyzed, 27 were present at Mata Comprida settlement, 26 at Laranjeira I, and 20 at Laranjeira II. Regarding the totality of all sandflies collected, 274, 201, and 155 were from Mata Comprida, Laranjeira II and I, respectively. Ny. whitmani was the most frequent (26.5%) followed by Ev. evandroi (16%), and Ev. termitophila (12.7%). Lutzomyia longipalpis and Lutzomyia cruzi, despite the low frequency (2.8%), were captured sympatrically. Two species of the genus Evandromyia were not identified at a specific level, which could be new species. Taxonomic studies will be performed aiming to verify this question, as well as the female of Brumptomyia mangabeirai (Table 1).
Nyssomyia whitmani predominated both in forest (SISA=0.98) and anthropic environments (SISA=0.94) and was in both ecotopes.
Ev. evandroi and Ev. termitophila, the second and the third most frequent species overall, were both in second position at forest environment (SISA=0.87) and anthropic environment (SISA=0.87), respectively. Only Evandromyia aldafalcaoae, Pintomyia nevesi, and Psychodopygus hirsutus were not captured in the forest environment (Table 2).
Table 3 shows that in every settlement, the amount of insects captured in forest environments were higher (p<0.01) than anthropic environments.
Otherwise, when the intradomicile and peridomicile of these settlements are compared, significant differences (p<0.01) were noted only at Laranjeira I settlement with a large amount of insects in peridomicile areas, as shown in Table 4.
DISCUSSION
Light trap captures allowed the identification of 630 sandflies belonging to 28 species, from 11 genera, confirming the large diversity of the phlebotomine sandfly fauna at these three settlements in the municipality of Cáceres, as already reported from other places in the State of Mato Grosso14-16.
According to Missawa and Maciel17 and Amaral et al.18, the variety of phlebotomine sandflies found in the State of Mato Grosso is as expected (107 species) considering the diversity of biomes characteristic of the region, such as savannah, Pantanal, transition forest, and the Amazon rainforest.
The data obtained in this research increased our knowledge of these insects fauna in the State, with six species not previously recorded: Brumptomyia avellari, Br. mangabeirai, Evandromyia aldafalcaoae, Micropygomyia echinatopharynx, Micropygomyia peresi, and Psathyromyia campograndensis, raising the current record of species in the State to 112.
Among the identified species, nine (43%) presented a wide geographic distribution in Brazil, with Evandromyia evandroi, Lutzomyia longipalpis, Nyssomyia whitmani, and Psathyromyia aragaoidocumented in the five Brazilian regions, and the species Brumptomyia avellari, Evandromyia termitophila, Micropygomyia peresi, Psathyromyia brasiliensis, and Psathyromyia hermanlenti are present in the north, northeast, southeast, and midwest regions of the country14. The wide area of occurrence of these species can be explained by their adaptation to diverse habitats.
When comparing the number of specimens of each environment (intra, peridomicile, and forest) at the three settlements, we can notice that at anthropized environments (170/27%), a lower percentage of insects was observed when compared with the forest environment (460/73%); the higher quantity found in the forest can be explained by the plentiful organic matter of the soil and as this is the natural habitat of these insects19. Still, we should consider that it is usual at transmission areas of cutaneous leishmaniasis (CL) to have a destruction of primary forests with subsequent invasion of vectors into the peridomicile environment20.
When the ratio of males to females is analyzed, we can notice the predominance of females with 0.81:1, contrasting with the result of the several works performed in the midwest region, which reported the reverse, such as Missawa and Dias21, that found a male predominance of 1.9:1 at Várzea Grande, MT; Galati et al.22 with 1.2:1 at Corumbá, State of Mato Grosso do Sul (MS); Almeida et al.23 with 4.8:1 at Ponta Porã, MS; and Nunes et al.24 with 5.7:1 at Bonito, MS.
Comparing the density of phlebotomine sandflies at the three ecotopes, it is possible to notice a superior frequency and variety of species at Mata Comprida settlement. It is suggested that the largest finding of species (27) and specimens (274) captured at this settlement was due to biotic factors relating to savannah. Also worth pointing out is that this location has banana plantations and various fruit trees, and breeding sites of birds, pigs, horses, and cattle.
Galati et al.25 and Oliveira et al.26 emphasized the relevance of a sty and chicken coop as places of creation and maintenance of the high density of phlebotomine sandflies in the environment as a risk factor, which should be considered by epidemiological surveillance when planning actions to control the disease.
The settlement Laranjeira II, where savannah is predominant, was the ecotope that presented the second highest index of population density (201) of insects. In this ecosystem, Ny. whitmani was found in greater numbers compared with the other two settlements, which could be a reflection of greater adaptation to the environment, as this area is the older ecotope (24 years). Few species identified at this place, such as Lutzomyia longipalpis, Evandromyia lenti, Nyssomyia whitmani, Psathyromyia shannoni, Micropygomyia quinquefer, Sciopemyia sordellii, and Ev. termitophila, were also described by Martin and Rebêlo27 from a savannah area at Maranhão.
The settlement Laranjeira I was the place with the lowest quantity of phlebotomine sandflies obtained (155) and with 79.3% of the species captured in the forest area. Of this number, only 32 specimens were attracted by traps set in the peridomicile area. It is a recent settlement located closer to the Boi Morto mountain range, and it is situated at a transition area with Pantanal. Possibly, the specimens still found food and shelter in areas of native forest. Furthermore, it is possible that the sandflies are undergoing adaptation and colonization. Another hypothesis is that the presence of a convex formation and fluvial plain promote high soil moisture due to flooding of the Paraguay River. It is known that this factor is prejudicial to the development of phlebotomine larvae28.
Among the species found in this study, we should emphasize Ny. whitmani, Lu. longipalpis, and Lutzomyia cruzi. The first two are efficient vectors of cutaneous and visceral leishmaniasis, respectively, and the last one is implicated as a visceral leishmaniasis (VL) vector. These species are anthropophilic and possess greater ability to adapt to environments modified by man1,29. This epidemiological aspect is important as it could explain some cases of a visceral form that occurred among the residents who live at the settlements.
This study indicated the predominance of Ny. whitmani, which is of public health concern, as this vector is incriminated as a major vector of Leishmania (Viannia) braziliensis in the south, southeast, northeast, and midwest regions of Brazil, and Leishmania (V.) shawi in the north30,31and Leishmania (V.) guyanensis in the Amazon32. It is an anthropophilic, exophilic insect frequently found in the forest and anthropized environments, with chicken coops and pig sties33,34. These characteristics were also observed in the present study area.
The species Ny. whitmani, besides being the most abundant overall (167/630), was most frequently found in the savannah (75.4%) as discovered in the State of Mato Grosso by Missawa e cols5. It is known that cutaneous leishmaniasis is a zoonosis of rural environments35,36 similar to the settlements studied here.
Despite the predominance of a forest area (74.2%) in the three settlements, Ny. whitmani was present in lower percentages at peridomicile environments (25.8%); however, it is worth noticing that this vector is opportunistic and has an eclectic habit for food, adjusting its eating habits to the availability of hosts at anthropic environments37. According to Souza et al.38, transmission of leishmaniasis can occur in intradomicile and peridomicile environments.
We should note the findings of Lu. longipalpis and Lu. cruzi in sympatry at the settlements Mata Comprida, Laranjeira I and II, similar to the one previously observed by Oliveira et al.34 at Campo Grande, MS. Missawa and Lima39 conducted studies at 68 of 139 municipalities in MT, and Lu. longipalpis was reported at 23 of these. This species was found at higher frequency in the savannah, Amazon rainforest, transition, and Pantanal environments, corroborating with the present study.
The finding of Lu. longipalpis at the settlement Mata Comprida at the forest and intradomicile environments, even in low quantity, represents a significant result as this species presents a high vectorial capacity, anthropophily, and an eclectic choice of hosts, besides being the major vector of Leishmania (Leishmania) infantum chagasi in the Americas, including Brazil29. The domiciliation of this vector at undeveloped rural areas has become greater due to the modification of the forests and anthropic action, mostly when associated with poor environmental sanitation and low socioeconomic status, as found at the settlements in question40-42.
The species Lu. cruzi has a wide geographic distribution at Mato Grosso, which is found in 24 municipalities but had not previously been reported from Cáceres39. Meanwhile, its finding at anthropized environments in Laranjeira II and Mata Comprida has epidemiological importance as it has previously been reported from Jaciara, MT43; Corumbá, MS; and Ladário, MS44. At these municipalities, cases of human and canine visceral leishmaniasis were reported in the absence of Lutzomyia longipalpis, and with a detection of natural infection of Lu. cruzi by Leishmania chagasiindicating, therefore, the participation of these phlebotomines in the transmission of the disease.
Evandromyia evandroi, Ev. termitophila, Ev. peresi, Br. avellari, and Ev. lenti were all frequently reported in areas close to the animal hosts. However, none of these species is associated with Leishmania spp.14 transmission, except Ev. lenti, which has been found naturally infected with Leishmania braziliensis, despite being refractory to experimental infection45,46.
The unorganized inhabitation of the environment that is occurring at the settlements Mata Comprida, Laranjeira I and II could lead to domiciliation of the wild population of phlebotomines, including the vectors of leishmaniasis. This highlights the need to carry out further studies to fully understand the dynamic transmission of these diseases in such places.
ACKNOWLEDGMENTS
The authors thank the residents of the settlements for their permission to carry out this research, the geographer Jaqueline Cochev for the creation of the map, and Josdemar Muniz de Moraes, Sebastião Rodrigues, and Clóvis de Campos Leite from the laboratory of the Regional Health Office of Cáceres (ERSC) for the logistic support. The authors would also like to extend their gratitude to Dr. Daniel Bray for the revision of the manuscript.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
FINANCIAL SUPPORT
This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior(CAPES).
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Address to:
Dra. Alessandra Gutierrez de Oliveira
Lab. Parasitologia Humana/CCBS/UFMS
Cidade Universitária s/n
79070-900 Campo Grande, MS, Brasil
Phone: 55 67 3345-7390
e-mail: alessandra.oliveira@ufms.br
Received in 29/07/2011
Accepted in 03/11/2011
